A reservoir of ‘historical’ antibiotic resistance genes in remote pristine Antarctic soils

BackgroundSoil bacteria naturally produce antibiotics as a competitive mechanism, with a concomitant evolution, and exchange by horizontal gene transfer, of a range of antibiotic resistance mechanisms. Surveys of bacterial resistance elements in edaphic systems have originated primarily from human-i...

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Main Authors: Van Goethem, Marc W, Pierneef, Rian, Bezuidt, Oliver KI, Van De Peer, Yves, Cowan, Don A, Makhalanyane, Thulani P
Format: Article in Journal/Newspaper
Language:unknown
Published: eScholarship, University of California 2018
Subjects:
Online Access:https://escholarship.org/uc/item/4kn746f2
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spelling ftcdlib:oai:escholarship.org:ark:/13030/qt4kn746f2 2023-10-01T03:51:56+02:00 A reservoir of ‘historical’ antibiotic resistance genes in remote pristine Antarctic soils Van Goethem, Marc W Pierneef, Rian Bezuidt, Oliver KI Van De Peer, Yves Cowan, Don A Makhalanyane, Thulani P 40 2018-12-01 application/pdf https://escholarship.org/uc/item/4kn746f2 unknown eScholarship, University of California qt4kn746f2 https://escholarship.org/uc/item/4kn746f2 public Microbiome, vol 6, iss 1 Genetics Infectious Diseases Antimicrobial Resistance Infection Life Below Water Antarctic Regions Anti-Bacterial Agents Bacteria Drug Resistance Multiple Bacterial Gene Transfer Horizontal Genes Membrane Transport Proteins Metagenomics Soil Microbiology Antibiotic resistance genes Soil resistome Antarctica Ecology Microbiology Medical Microbiology article 2018 ftcdlib 2023-09-04T18:04:53Z BackgroundSoil bacteria naturally produce antibiotics as a competitive mechanism, with a concomitant evolution, and exchange by horizontal gene transfer, of a range of antibiotic resistance mechanisms. Surveys of bacterial resistance elements in edaphic systems have originated primarily from human-impacted environments, with relatively little information from remote and pristine environments, where the resistome may comprise the ancestral gene diversity.MethodsWe used shotgun metagenomics to assess antibiotic resistance gene (ARG) distribution in 17 pristine and remote Antarctic surface soils within the undisturbed Mackay Glacier region. We also interrogated the phylogenetic placement of ARGs compared to environmental ARG sequences and tested for the presence of horizontal gene transfer elements flanking ARGs.ResultsIn total, 177 naturally occurring ARGs were identified, most of which encoded single or multi-drug efflux pumps. Resistance mechanisms for the inactivation of aminoglycosides, chloramphenicol and β-lactam antibiotics were also common. Gram-negative bacteria harboured most ARGs (71%), with fewer genes from Gram-positive Actinobacteria and Bacilli (Firmicutes) (9%), reflecting the taxonomic composition of the soils. Strikingly, the abundance of ARGs per sample had a strong, negative correlation with species richness (r = - 0.49, P < 0.05). This result, coupled with a lack of mobile genetic elements flanking ARGs, suggests that these genes are ancient acquisitions of horizontal transfer events.ConclusionsARGs in these remote and uncontaminated soils most likely represent functional efficient historical genes that have since been vertically inherited over generations. The historical ARGs in these pristine environments carry a strong phylogenetic signal and form a monophyletic group relative to ARGs from other similar environments. Article in Journal/Newspaper Antarc* Antarctic Antarctica University of California: eScholarship Antarctic Mackay ENVELOPE(168.517,168.517,-77.700,-77.700) Mackay Glacier ENVELOPE(162.000,162.000,-76.967,-76.967)
institution Open Polar
collection University of California: eScholarship
op_collection_id ftcdlib
language unknown
topic Genetics
Infectious Diseases
Antimicrobial Resistance
Infection
Life Below Water
Antarctic Regions
Anti-Bacterial Agents
Bacteria
Drug Resistance
Multiple
Bacterial
Gene Transfer
Horizontal
Genes
Membrane Transport Proteins
Metagenomics
Soil Microbiology
Antibiotic resistance genes
Soil resistome
Antarctica
Ecology
Microbiology
Medical Microbiology
spellingShingle Genetics
Infectious Diseases
Antimicrobial Resistance
Infection
Life Below Water
Antarctic Regions
Anti-Bacterial Agents
Bacteria
Drug Resistance
Multiple
Bacterial
Gene Transfer
Horizontal
Genes
Membrane Transport Proteins
Metagenomics
Soil Microbiology
Antibiotic resistance genes
Soil resistome
Antarctica
Ecology
Microbiology
Medical Microbiology
Van Goethem, Marc W
Pierneef, Rian
Bezuidt, Oliver KI
Van De Peer, Yves
Cowan, Don A
Makhalanyane, Thulani P
A reservoir of ‘historical’ antibiotic resistance genes in remote pristine Antarctic soils
topic_facet Genetics
Infectious Diseases
Antimicrobial Resistance
Infection
Life Below Water
Antarctic Regions
Anti-Bacterial Agents
Bacteria
Drug Resistance
Multiple
Bacterial
Gene Transfer
Horizontal
Genes
Membrane Transport Proteins
Metagenomics
Soil Microbiology
Antibiotic resistance genes
Soil resistome
Antarctica
Ecology
Microbiology
Medical Microbiology
description BackgroundSoil bacteria naturally produce antibiotics as a competitive mechanism, with a concomitant evolution, and exchange by horizontal gene transfer, of a range of antibiotic resistance mechanisms. Surveys of bacterial resistance elements in edaphic systems have originated primarily from human-impacted environments, with relatively little information from remote and pristine environments, where the resistome may comprise the ancestral gene diversity.MethodsWe used shotgun metagenomics to assess antibiotic resistance gene (ARG) distribution in 17 pristine and remote Antarctic surface soils within the undisturbed Mackay Glacier region. We also interrogated the phylogenetic placement of ARGs compared to environmental ARG sequences and tested for the presence of horizontal gene transfer elements flanking ARGs.ResultsIn total, 177 naturally occurring ARGs were identified, most of which encoded single or multi-drug efflux pumps. Resistance mechanisms for the inactivation of aminoglycosides, chloramphenicol and β-lactam antibiotics were also common. Gram-negative bacteria harboured most ARGs (71%), with fewer genes from Gram-positive Actinobacteria and Bacilli (Firmicutes) (9%), reflecting the taxonomic composition of the soils. Strikingly, the abundance of ARGs per sample had a strong, negative correlation with species richness (r = - 0.49, P < 0.05). This result, coupled with a lack of mobile genetic elements flanking ARGs, suggests that these genes are ancient acquisitions of horizontal transfer events.ConclusionsARGs in these remote and uncontaminated soils most likely represent functional efficient historical genes that have since been vertically inherited over generations. The historical ARGs in these pristine environments carry a strong phylogenetic signal and form a monophyletic group relative to ARGs from other similar environments.
format Article in Journal/Newspaper
author Van Goethem, Marc W
Pierneef, Rian
Bezuidt, Oliver KI
Van De Peer, Yves
Cowan, Don A
Makhalanyane, Thulani P
author_facet Van Goethem, Marc W
Pierneef, Rian
Bezuidt, Oliver KI
Van De Peer, Yves
Cowan, Don A
Makhalanyane, Thulani P
author_sort Van Goethem, Marc W
title A reservoir of ‘historical’ antibiotic resistance genes in remote pristine Antarctic soils
title_short A reservoir of ‘historical’ antibiotic resistance genes in remote pristine Antarctic soils
title_full A reservoir of ‘historical’ antibiotic resistance genes in remote pristine Antarctic soils
title_fullStr A reservoir of ‘historical’ antibiotic resistance genes in remote pristine Antarctic soils
title_full_unstemmed A reservoir of ‘historical’ antibiotic resistance genes in remote pristine Antarctic soils
title_sort reservoir of ‘historical’ antibiotic resistance genes in remote pristine antarctic soils
publisher eScholarship, University of California
publishDate 2018
url https://escholarship.org/uc/item/4kn746f2
op_coverage 40
long_lat ENVELOPE(168.517,168.517,-77.700,-77.700)
ENVELOPE(162.000,162.000,-76.967,-76.967)
geographic Antarctic
Mackay
Mackay Glacier
geographic_facet Antarctic
Mackay
Mackay Glacier
genre Antarc*
Antarctic
Antarctica
genre_facet Antarc*
Antarctic
Antarctica
op_source Microbiome, vol 6, iss 1
op_relation qt4kn746f2
https://escholarship.org/uc/item/4kn746f2
op_rights public
_version_ 1778517302284648448